Invasion Risks Posed by Ornamental Freshwater Fish Trade to Southeastern Brazilian Rivers

Invasion risks posed by ornamental freshwater fish trade to southeastern Brazilian rivers

André Lincoln Barroso de Magalhães1 and Claudia Maria Jacobi2

A model was developed to assess the risk of invasion of ornamental non-native fishes to six rivers in the state of Minas Gerais, southeastern Brazil, with focus on species popularity. Thirty-nine aquarium shops, in six cities, were visited monthly from January to December 2007. In each city, fish species were identified, and their biology and invasion history information was obtained from the literature. We calculated the annual frequency of occurrence and average number of specimens monthly available in stores. Quarterly water temperature and dissolved oxygen data from 1997 to 2007 were obtained for the Velhas, Muriaé, Uberabinha, Sapucaí-Mirim, Doce and Todos os Santos Rivers from public databases. The invasion risk of each species was assessed through a model comprising nine parameters grouped in four variables: (i) Invasiveness (thermal and dissolved oxygen ranges, diet, parental care or fecundity), (ii) History of invasions (establishment), (iii) Propagule pressure (commercial success, comprising annual frequency of occurrence and number of specimens available monthly at stores), and (iv) Invasibility (water temperature and dissolved oxygen in the target river compatible with the species ranges). Of the 345 ornamental fish species for sale, 332 are non-native to either Minas Gerais (n = 151) or Brazil (n = 194). Based on the proposed cutting values, in particular the compatibility between species and recipient thermal ranges, five ornamental non-native species (Cyprinus rubrofuscus, Carassius auratus, Xiphophorus hellerii, Poecilia reticulata, and P. latipinna) can potentially invade the Velhas and Muriaé Rivers, four species (Cyprinus rubrofuscus, Carassius auratus, X. helleri, and P. reticulata) the Uberabinha River, four species (Cyprinus rubrofuscus, Carassius auratus, X. maculatus, and P. reticulata) the Sapucaí-Mirim River, three species (Carassius auratus, X. hellerii, and P. reticulata) the Doce River, and three species (Cyprinus rubrofuscus, P. reticulata, and Amatitlania nigrofasciata) can potentially invade the Todos os Santos River. Six recommendations are suggested to reduce the invasion risk of non-native fish on the rivers surveyed posed by aquarium trade.

Um modelo foi desenvolvido para avaliar o risco de invasão de peixes ornamentais não-nativos em seis rios do estado de Minas Gerais, sudeste do Brasil, com foco na popularidade das espécies. Trinta e nove lojas de aquário em seis cidades foram visitadas mensalmente de janeiro a dezembro de 2007. Em cada cidade, as espécies foram identificadas e suas biologias e histórias de invasão foram obtidas da literatura. Calculou-se a frequência de ocorrência anual e quantidade média mensal de exemplares disponíveis nas lojas. Foram obtidas temperaturas trimestrais da água e dados de oxigênio dissolvido de 1997 a 2007 dos rios Velhas, Muriaé, Uberabinha, Sapucaí-Mirim, Doce e Todos os Santos a partir de bases de dados públicas. O risco de invasão de cada espécie foi avaliado através de um modelo composto por nove parâmetros agrupados em quatro variáveis: (i) Invasividade (limite de alcance térmico/oxigênio dissolvido, dieta, cuidado parental ou fecundidade), (ii) Histórico de invasões (estabelecimento), (iii) Pressão de propágulos (sucesso comercial, composto pela frequência de ocorrência anual e número de exemplares disponíveis mensalmente nas lojas), e (iv) Invasibilidade (temperatura da água/oxigênio dissolvido dos rios compatível com o limite de alcance térmico/ oxigênio dissolvido das espécies). Das 345 espécies de peixes ornamentais para venda, 332 são não-nativos para Minas Gerais (n = 151) ou Brasil (n = 194). Com base nos valores de corte propostos, cinco espécies de peixes ornamentais não-nativos (Cyprinus rubrofuscus, Carassius auratus, Xiphophorus hellerii, Poecilia reticulata e P. latipinna) podem potencialmente invadir os rios Velhas e Muriaé, quatro espécies (C. rubrofuscus, C. auratus, X. helleri, P. reticulata) podem invadir o rio Uberabinha, quatro espécies selecionadas (Cyprinus rubrofuscus, Carassius auratus, X. maculatus e P. reticulata) podem invadir o rio Sapucaí-Mirim, três espécies (Carassius auratus, X. hellerii e P. reticulata) podem invadir o rio Doce, e três espécies (Cyprinus rubrofuscus, P. reticulata e Amatitlania nigrofasciata) podem potencialmente invadir o rio Todos os Santos. Seis recomendações são sugeridas para reduzir o risco de invasão por peixes não-nativos nos rios pesquisados, representado pelo comércio de peixes ornamentais.

Key words: Aquarium shops, Aquarium dumping, Fishkeeping, Invasion risk assessment, Non-native fishes.

1Universidade Federal de Minas Gerais, Programa de Pós-Graduação em Ecologia, Conservação e Manejo de Vida Silvestre, Av. Antônio Carlos, Pampulha, 6627, 31270-901 Belo Horizonte, MG, Brazil. [email protected] 2Universidade Federal de Minas Gerais, Departamento de Biologia Geral, Instituto de Ciências Biológicas, Av. Antônio Carlos, Pampulha, 6627, 31270-901 Belo Horizonte, MG, Brazil. [email protected]

433 434 Invasion risks posed by ornamental freshwater fish trade

Introduction Material and Methods

Worldwide, keeping freshwater and marine ornamental fish Predicting potential invaders in six rivers of Minas Gerais in aquaria is a popular hobby in both homes and public spaces. State. A model was applied to predict probable non-native fish Currently, the global ornamental fish trade generates about invasions through aquarium fish trade in rivers of Minas Gerais US$ 3 billion/year and an equipment and literature industry State. This southeastern Brazilian state is the fourth in size, that exceeds US$ 15 billion/year (Dawes, 2001). In spite of the and the second most populous, with a current population of popularity of fishkeeping, not all amateurs persevere in more than 18 million (Alves et al., 2007). A donor source of adequately caring for their aquaria due to unwelcome species, represented by ornamental fish trade, was identified difficulties such as excessive growth of individuals and and adopted as a vector for deliberate human dumping, in order aggressiveness of some species. Upon giving up their hobby, to create a predictive model that combined biological, historical, many aquarium owners are reluctant to sacrifice their pets, and commercial variables, as proposed by Rixon et al. (2005), and end up discarding them directly in artificial (Fuller et al., with abiotic criteria, as proposed by Chang et al. (2009). 1999) and natural environments (Semmens et al., 2004). The first of these four variables is the invasiveness ability Aquarium dumping, according to Fuller et al. (1999), is of each species, assessed by four parameters: thermal range, the second main cause of non-native species introduction in dissolved oxygen tolerance, type of diet, and parental care or the US. In Brazil, most of the information about fish fecundity (representing reproductive attributes). The introductions concerns escapees from fish farms for food attributes assumed to facilitate the invasion of ornamental production, while reports of aquarium dumping are rare fish were the ability to tolerate changes in water temperature (Magalhães, 2010). Attention has been paid to non-native and dissolved oxygen levels, omnivorous diet (feeding on at ornamental fish species in Brazil, as well as elsewhere in the least two items among organic debris, micro- or macrophytes, world, only after they have settled into a new environment micro- or macro-invertebrates) and either parental care (by (Alves et al., 2007). Once established, it becomes virtually male, female, or both) or high fecundity (high numbers of impossible to eradicate aquatic species (Gozlan et al., 2010). oocytes). These are important prerequisites for the In order to prevent future invasions in Brazilian water bodies establishment of ornamental non-native species in any via aquarium trade, it is necessary to identify species of freshwater body (Moyle & Marchetti, 2006). The second ornamental fish that pose high invasion risks, as well as to variable is the history of worldwide invasions, adapted from monitor the events that may lead to these introductions (such Drake (2007), defined as H = Pe/Pi ×100, where H = history of as new species offered by the market, environmental changes, invasions, Pe = number of countries where the species has and urban growth). successfully established itself, Pi = number of countries where According to Bomford & Glover (2004), simple risk the species was introduced. The third variable is propagule assessment models that predict invasion risk by non-native pressure, estimated by the number of individuals released, a species are a low-cost alternative to guide management primary factor in establishment success (Vander Zanden & policies. Risk models were originally developed to deal with Olden, 2008). Assuming that popular species (i.e. hardy and chemical pollution, and have only recently been adapted for easy to feed) sold in considerable numbers (> 100 specimens other stressors, including non-native species (Calado & per month) have a greater probability of being released in the Chapman, 2006). Invasion risk models by non-native environment by hobbyists, we used the annual frequency of ornamental fish exist for temperate regions, such as those of occurrence in stores, and number of specimens of each species Gertzen et al. (2008), Kolar & Lodge (2002), Rixon et al. (2005), available monthly for sale as measures of commercial success. Chang et al. (2009), Strecker et al. (2011) for North America, The fourth variable is invasibility of the recipient river, and for sub-tropical/tropical regions such as the one assessed as the compatibility of its water temperature range developed by Bomford & Glover (2004) for Oceania. (mean autumn-winter and spring-summer, Table 1) with the Kaplan & Garrick (1981) define risk as the probability of thermal ranges tolerated by the invading species, as proposed ocurrence of an unwanted event, along with an assessment by Chang et al. (2009). Dissolved oxygen was also assessed of its consequences. In the case of aquarium trade, the because urban portions of most Brazilian rivers are usually undesired event is the release of non-native ornamental fish polluted by domestic and industrial sewage and would be by hobbyists, while consequences include establishment less suitable for fish survival (IGAM, 2009). All these variables through reproduction in new environments and ensuing are important steps in successful biological invasions by damages such as changes in the original structure of native aquatic species according to Lockwood et al. (2007). To be fish communities. Our study applies for the first time a simple considered a potential invasive species in any of the six rivers, risk model of ornamental non-native fish invasion in a species had to fulfill rigorously the cutting values of all four southeastern Brazil, based on species biological traits and variables and nine parameters described above (Table 2). invasion history, popularity, availability, and abiotic features of the recipient environment, along with a discussion of Data sampling and analysis aquarium dumping consequences and recommendations to Nineteen aquarium shops were visited monthly from restrain this practice. January to December 2007 in the city of Belo Horizonte (Velhas A. L. B. Magalhães & C. M. Jacobi 435

Table 1. Water temperature and dissolved oxygen (mean ± and Teófilo Otoni, and approximately to 90% in Belo SD) of the six target rivers in Minas Gerais State, from 1997 to Horizonte, Uberlândia and Governador Valadares. This 2007. Source: IGAM (2009). estimate was obtained consulting the specific store directory records of each city. The rivers were chosen because part of River (watershed) Autumn-winter Spring-summer 22.0 ± 2.1oC 25.1 ± 1.5oC their course is within these urban areas, where dumping is Velhas (São Francisco) 6.6 ± 1.1 mg/L 6.1 ± 0.4 mg/L more likely. We calculated the annual frequency of occurrence 23.0 ± 1.5oC 26.4 ± 0.6oC Muriaé (Paraíba do Sul) and the monthly average number of fish for sale at stores in 7.5 ± 0.3 mg/L 6.7 ± 0.4 mg/L each region. 22.7 ± 1.3oC 25.9 ± 1.0oC Uberabinha (Paranaíba) 6.4 ± 0.3 mg/L 6.2 ± 0.2 mg/L The common and scientific names of all species were 19.0 ± 2.0oC 22.4 ± 1.6oC recorded in the aquarium shops, and keys or distinguishing Sapucaí-Mirim (Grande) 7.6 ± 0.4 mg/L 6.4 ± 0.3 mg/L characteristics were compared and confirmed with those in 22.0 ± 0.6oC 25.2 ± 0.1oC Doce (Doce) Fryer & Iles (1972), Géry (1977), Rosen (1979), Merrick & 7.8 ± 0.2 mg/L 7.1 ± 0.1 mg/L 23.6 ± 1.1oC 26.5 ± 1.4oC Schmida (1984), Burgess (1989), Page & Burr (1991), Talwar & Todos os Santos (Mucuri) 7.0 ± 0.2 mg/L 6.3 ± 0.5 mg/L Jhingran (1992), Kottelat et al. (1993), Kullander & Hartel (1997), and Nelson (2006). Color photographs of live species in Axelrod et al. (1997) were used to confirm specimens. River, São Francisco River basin), four in the city of Muriaé Information regarding thermal ranges, diet, reproduction, (Muriaé River, Paraíba do Sul River basin), four in Uberlândia worldwide invasion events were obtained from the reliable (Uberabinha River, Paranaíba River, upper Paraná River basin), website Froese & Pauly (2006) for most of the species. The four in Pouso Alegre (Sapucaí-Mirim River, Grande River, thermal range of Carassius auratus was obtained from Ford upper Paraná River basin), four in Governador Valadares (Doce & Beitinger (2005), the diet of T. lalius and T. leeri, and the River, Doce River basin) and four in Teófilo Otoni (Todos os fecundity of P. conchonius were obtained respectively from Santos River, Mucuri River basin) (Fig. 1). The number of Richter (1988), Degani (1990) and Çek & Gökçe (2005). The stores surveyed corresponds to 100% in Muriaé, Pouso Alegre threshold of dissolved oxygen considered acceptable for

Table 2. Cutting values of parameters used in the model. Sources: Richter (1988), Degani (1990), Lawson (1995), Ford & Beitinger (2005), Çek & Gökçe (2005), Froese & Pauly (2006).

Parameters No/Low risk Yes/High risk Invasiveness Thermal range tolerance < 6.0oC ≥ 6.0oC ≥ 5.0 mg/L (warm water species) < 5.0 mg/L (warm water species) Minimum of dissolved oxygen ≥ 6.0 mg/L (cold water species) < 6.0 mg/L (cold water species) Type of diet 1 food category (invertivore/herbivore) > 1 food category (omnivore) Parental care No parental care ≥ 1 type (parental care) Fecundity < 100.000 oocytes (low fecundity) ≥ 100.000 oocytes (high fecundity) Invasion history Pe/Pi×100 < 50 % (countries) ≥ 50 % (countries) Propagule pressure Frequency of occurrence (FO) < 50 % (FO in stores) ≥ 50 % (FO in stores) Numbers available for sale/month < 100 individuals (sold/month) ≥ 100 individuals (sold/month) Invasibility Water temperature (mean) Velhas < 22.0 or > 25.1oC 22.0 - 25.1oC Muriaé < 23.0 or > 26.4oC 23.0 - 26.4oC Uberabinha < 23.7 or > 25.9oC 22.7 - 25.9oC Sapucaí-Mirim < 19.0 or > 22.4oC 19.0 - 22.4oC Doce < 22.0 or > 25.2oC 22.0 - 25.2oC Todos os Santos < 23.6 or > 26.5oC 23.6 - 26.5oC 436 Invasion risks posed by ornamental freshwater fish trade

the striped catfish Pangasianodon hypophthalmus and the clown knifefish Chitala ornata), aggressive (the golden mbuna Melanochromis auratus and the giant snakehead Channa micropeltes), expensive (the discus fish Symphysodon discus and the sixbar distichodus Distichodus sexfasciatus), and rare species (the short-tailed pipefish Microphis brachyurus and the marble goby Oxyeleotris marmorata) were available in less than 50% of the stores. Based on the model proposed (Fig. 2) only seven non-native species may potentially invade and establish themselves in the rivers surveyed if dumped by hobbyists, and most of them are common to several rivers. Five non-native species (Cyprinus rubrofuscus, Carassius auratus, X. hellerii, and P. reticulata, P. latipinna) are a threat to both the Velhas and Muriaé Rivers. In the Uberabinha River we found four potential invaders (Cyprinus rubrofuscus, Carassius auratus, X. hellerii, and P. reticulata), Fig. 1. Cities and watersheds within the Minas Gerais State, four in the Sapucaí-Mirim River (Cyprinus rubrofuscus, Carassius Brazil, where the 39 ornamental fish stores were visited. auratus, X. maculatus, and P. reticulata), three (Carassius auratus, X. hellerii, and P. reticulata) in the Doce River, and three species (Cyprinus rubrofuscus, P. reticulata, and Amatitlania nigrofasciata) in the Todos os Santos River (Table freshwater fish was taken from Lawson (1995). 3). Quarterly data from 1997 to 2007 of water temperature The model excluded M. anguillicaudatus (Muriaé), B. and dissolved oxygen for the six rivers were obtained from splendens (Velhas, Muriaé, Uberabinha, Sapucaí-Mirin, Doce, the public database of the Minas Gerais Institute of Water and Todos os Santos), X. hellerii (Sapucaí-Mirim), X. Management (IGAM) (2009). Water temperature (ºC; maculatus (Velhas, Muriaé, Uberabinha, Doce, and Todos os thermometer) and dissolved oxygen (mg/L; Winkler’s method Santos), T. lalius (Velhas and Muriaé), G. ternetzi, Pethia by Golterman et al., 1978) were measured downstream and conchonius, Puntius semifasciolatus (Velhas and Muriaé), T. upstream of each city (average distance: 19,8 ± 11,6 km) at 1 m trichopterus (Velhas, Muriaé, Uberabinha, Grande, and Doce), depth in the main channel of each river. T. leeri (Velhas), and Maylandia lombardoi (Muriaé) as potential invaders because none of these 11 species have a Results thermal range compatible with the recipient environments. In addition, M. anguillicaudatus, B. splendens, T. lalius, G. We found 345 species of ornamental fish belonging to ternetzi, T. trichopterus, and T. leeri are not omnivorous, and 58 families on sale at stores, of which 332 were non-native M. anguillicaudatus, G. ternetzi, P. conchonius and P. either to the watersheds studied (151 species from the semifasciolatus lack parental care, have low fecundity or Pantanal and Amazonian basins) or to Brazil (194 species absence of data. Also, T . trichopterus and M. lombardoi from North America, Central America, South America, Africa, were available in very low amounts. On the other hand, Asia, and Oceania). In Belo Horizonte we recorded 166 fish dissolved oxygen levels were adequate in all sites, and did species (five native and 161 non-native) belonging to 37 not discriminate species (Table 3). families, with an average number of 40.2 ± 30.2 species per store. In Muriaé, we recorded 52 species (eight native and Discussion 44 non-native) belonging to 15 families, with an average number of 33.7 ± 7.7 species per store. In Uberlândia, 83 Our survey of ornamental fish stores in Minas Gerais State species (all of which non-native) belonging to 16 families showed that the number of species available for sale is were found, with an average of 26.3 ± 16.7 species. We relatively large (n = 345), and that although these species are recorded 29 species (all of which non-native) belonging to of tropical origin, the great majority is non-native to the state seven families in Pouso Alegre, with an average of 11.1 ± 0.5 or country (96,23%). For these reasons, their trade as an species per store. In Governador Valadares, we found 15 introduction pathway deserves better investigation and species (all of them non-native) belonging to six families, regulation by environmental authorities. Concern about the with an average of 10.2 ± 3.5 species per store and finally, in predominance of non-native fishes in aquarium trade was Teófilo Otoni, 14 species (all of them non-native) belonging recently addressed by Gertzen et al. (2008) in Canada, and by to five families, with an average of 10.4 ± 2.5 species per Chang et al. (2009) and Strecker et al. (2011) in the states of store. Fishes well-known by hobbyists such as cyprinids, California and Washington, US. Of 252, 432 and 400 species poeciliids, and osphronemids, all with non-native available at stores in the respective regions surveyed by these representatives, were the most traded. Usually large (e.g., authors, the absolute majority was of tropical origin. A. L. B. Magalhães & C. M. Jacobi 437

In our survey, Cyprinidae, Poeciliidae, and Osphronemidae were the most popular families in stores. A similar trend was found by Duggan et al. (2006) in Toronto, Canada, and Macomb County, Michigan, US. According to these authors, popular families available to hobbyists have a tendency to be introduced more frequently and in greater numbers than rare families. Members of these ‘high-risk’ families are usually sturdy, have low aggressiveness, and are small enough to be kept in large numbers, thus adding to propagule pressure. Some exceptions are Cyprinus rubrofuscus and Carassius auratus, which are comparatively large, yet sold in large numbers. Most of these sales, however, are of juveniles, and both species have high indices of rejection when they attain their adult size. The model created for Minas Gerais State predicts that only four poeciliids, two cyprinids, and one cichlid are potential invaders of the six rivers surveyed. These families were also highlighted by Bomford & Glover (2004), whose model for the Australian tropical region identified poeciliids and cyprinids as the highest risk taxa, followed by cichlids, which posed moderate risk. The very short list of potential invaders, when compared to the number of available non-natives, is the result of several restrictive model parameters, and mainly of the mismatch between species thermal ranges and the recipient river temperature. This rigorous selection also occurs in the model proposed by Chang et al. (2009), which detected five potential invasive species for the cold scenario (autumn-winter) in the San Francisco Delta Bay, California, and 27 species for the warm scenario (spring-summer). However, when both scenarios were considered, only five ornamental species were qualified as potential invaders. Aside from the thermal incompatibility discussed above, diet, parental care, fecundity, and number os specimens for sale contributed to eliminate 11 other species as potential invaders. Fish species that have thermal ranges incompatible with the location to be invaded, affecting embryo and egg development (Milton & Arthington, 1983), that have specialized feeding habits, lack parental care, have low fecundity (Moyle & Marchetti, 2006), and are commercially undesired by humans (Duggan et al., 2006), are seldom considered potential invaders (Strecker et al., 2011). Except for Cyprinus rubrofuscus (common variety) and P. reticulata introduced in the Velhas River (unknow introduction pathways, no evidence of reproduction) (Alves & Pompeu, 2001), there are no published records regarding the introduction of Carassius auratus, Cyprinus rubrofuscus - koi, P. latipinna, X. maculatus, X. hellerii, and A. nigrofasciata in this river. Similarly, there are no records regarding the introduction of Carassius auratus, Cyprinus rubrofuscus - koi, P. reticulata, P. latipinna, X. maculatus, X. hellerii, and A. nigrofasciata in Muriaé, Uberabinha, Sapucaí- Mirim, Doce and Todos os Santos Rivers. There are also no records of introduction of A. nigrofasciata in other sites in Fig. 2. A model describing the invasion stages that species Brazil. Of the seven potential invaders traded in Minas Gerais must pass in order to represent an invasion risk for rivers in and detected by the model, Carassius auratus, P. reticulata, Minas Gerais State, Brazil. X. maculatus, and X. hellerii have been introduced by 438 Invasion risks posed by ornamental freshwater fish trade

Table 3. Biological, historical and species frequency/numbers variables in 39 stores surveyed in Minas Gerais State. Only species with at least 50% occurrence are listed, in decreasing order of annual frequency of occurrence (FO). Cities: B = Belo Horizonte, M = Muriaé, U = Uberlândia, P = Pouso Alegre, G = Governador Valadares, T = Teófilo Otoni. Sources: Richter (1988), Degani (1990), Lawson (1995), Ford & Beitinger (2005), Çek & Gökçe (2005), Froese & Pauly (2006).

Annual FO (%) in all stores Thermal range (oC) and Reproductive Invasion Common name and numbers available for Cities dissolved oxygen (mg/L) Diet attributes history (%) Scientific name sale monthly in all stores (in (in brackets) brackets) koi carp B, M, U, P, 3-35 (6.0) omnivore high fecundity 52.30 91.25 (937.4 ± 177.8) Cyprinus rubrofuscus T pond loach M 5-25 (6.0) invertivore no parental care 88.89 89.58 (224.2 ± 218.4) Misgurnus anguillicaudatus low fecundity

Siamese fighting fish B, M, U, P, 24-30 (5.0) invertivore uniparental care (♂) 44.44 88.29 (112.4 ± 199.6) Betta splendens G, T goldfish B, M, U, P, 0-41 (6.0) omnivore high fecundity 79.31 86.18 (1095.7 ± 236.4) Carassius auratus G green swordtail B, M, U, P, 22-28 (5.0) omnivore uniparental care (♀) 67.74 80.50 (787.2 ± 140.5) Xiphophorus hellerii G southern platyfish B, M, U, P, 18-25 (5.0) omnivore uniparental care (♀) 65.00 79.61 (724.7 ± 156.6) Xiphophorus maculatus G, T guppy B, M, U, P, 18-28 (5.0) omnivore uniparental care (♀) 72.13 78.09 (586.8 ± 155.5) Poecilia reticulata G, T dwarf gourami B, M 25-28 (5.0) invertivore uniparental care (♂) 50.00 76.20 (342.4 ± 104.2) Trichogaster lalius black tetra B, M 20-26 (5.0) invertivore no parental care 50.00 73.63 (449.1 ± 217.9) Gymnocorymbus ternetzi fecundity not available rosy barb B, M 18-22 (5.0) omnivore no parental care 50.00 71.71 (292.6 ± 132.1) Pethia conchonius low fecundity three spot gourami B, M, U, P, 22-28 (5.0) invertivore uniparental care (♂) 58.33 71.67 (99.7 ± 143.3) Trichopodus trichopterus G

Chinese barb B, M 18-24 (5.0) omnivore no parental care 50.00 69.19 (317.4 ± 114.1) Puntius semifasciolatus low fecundity sailfin molly B, M 20-28 (5.0) omnivore uniparental care (♀) 76.92 68.80 (417.3 ± 121.9) Poecilia latipinna convict cichlid T 20-36 (5.0) omnivore biparental care 70.00 66.67 (331.2 ± 175.1) Amatitlania nigrofasciata pearl gourami B 24-28 (5.0) invertivore uniparental care (♂) 60.00 51.32 (150.7 ± 47.7) Trichopodus leerii cobalt M 24-26 (5.0) omnivore uniparental care (♀) 100.00 50.00 (6.2 ± 5.0) Maylandia lombardoi

hobbyists (with no evidence of reproduction) in the São introduced and is reproducing in the São Francisco and Doce Francisco River basin (X. hellerii) (Chaves & Magalhães, River basins respectively (Magalhães, 2008). These data attest 2010), in the Paraíba do Sul River basin (Carassius auratus, P. the imminent risk of invasion posed by aquarium dumping reticulata, X. maculatus, and X. hellerii) (Melo et al., 2006; and reinforce the need of aquarium trade regulation in Minas Alves et al., 2007), in the Doce River basin (Carassius auratus Gerais State. Cyprinus rubrofuscus (common variety) that and X. hellerii) (Alves et al. 2007), in the Jequitinhonha River escaped from fish farms has great importance in commercial basin (P. reticulata) (Neto, 2010), and in the Mucuri River fishing in several lotic and lentic environments in the Doce basin (P. reticulata) (Pompeu, 2010). P. reticulata was also River basin (Vieira, 2010). The same trend of spread may occur A. L. B. Magalhães & C. M. Jacobi 439 with Cyprinus rubrofuscus - koi if released by hobbyists in may cause on the water bodies of Minas Gerais State is by the studied rivers. Feral koi carp released by aquarium better informing those involved in this market, such as sectors amateurs has established itself and dispersed in a number of dealing with importation, breeding, transportation and trading rivers and lakes of New Zealand (Tempero et al., 2006). There of aquarium fish, as well as hobbyists. are no studies showing the adverse ecological effects of To put this into practice, we suggest the following introducing Cyprinus rubrofuscus - koi, Carassius auratus, recommendations for aquarium trade in Minas Gerais State, P. latipinna, X. maculatus, and X. hellerii by hobbyists in and Brazil as a whole: (i) instruct suppliers and retailers to sell Minas Gerais or elsewhere in Brazil. On the other hand, the only males of the potential invader cyprinids Cyprinus ecological effects of P. reticulata are known not only in the rubrofuscus - koi (veil variety), Carassius auratus (veiltail, state but other locations in Brazil: this poeciliid has negatively telescope-eye, bubble-eye and celestial-eye varieties) and changed fish community structures in streams of southern poeciliids Xiphophorus hellerii, X. maculatus, Poecilia Brazil (Vieira & Shibatta, 2007; Cunico et al., 2009). reticulata, P. latipinna (veiltail and lyretail varieties) and female The model selected relatively few species as potential of the cichlid A. nigrofasciata (striped variety). These are more invaders because it requires that all nine parameters be met, colorful (cyprinids, poeciliids, cichlid) and swim with difficulty but according to Chang et al. (2009), this does not mean that due to the long fins (cyprinids, poeciliids) or have protuberant the risk may be low. Firstly, the list of potential invading eye bulbs (Carassius auratus), which renders them more species is constantly increasing due to the aquarium trade susceptible to native predators; (ii) inform hobbyists of proper search for new species that appeal to its customers. Recent locations to hand over their fish (Brazilian federal or state examples are the cichlids, the flowerhorn Amphilophus environmental agencies, return to the fish farm or aquarium trimaculatum (= ‘Cichlasoma’ trimaculatum) × Amphilophus shop), thus avoiding indiscriminate dumping in nature; (iii) citrinellum, the black diamond cichlid Paratilapia polleni, with the assistance of qualified personnel, identify species that and the freshwater stingrays Potamotrygon spp. (A. L. B. may be used as viable alternatives in each region without risks Magalhães, pers. obs.). Secondly, there are presently in the of invasion; (iv) acknowledge and apply laws of fish import state more than 2,000 dammed water bodies (Alves et al., and quarantine; (v) inform the hobbyist about the species 2007), many located in the surroundings of the six cities characteristics when young and adult, so as to reduce rejection studied. Impoundments often exhibit marked fluctuations in and fish dumping, and allow for proper care; (vi) display posters nutrient content, a condition that increases invasibility for and flyers informing about “non-native species”, along with a aquarium fishes pre-adapted to lacustrine environments notice in bags, packaging paper and website (if any) of the (Magalhães, 2010). Lastly, with the demographic growth of aquarium shop. This notice must inform customers that in case the six cities in the last ten years, together with the aquarium they no longer want their fishes, they should never free them hobby expansion in Minas Gerais and Brazil (ANFALPET, in either natural (creeks, streams, rivers or lakes) or artificial 2010), the frequency of introductions and subsequent water bodies (channels, ponds or dams). establishment of aquarium fish species through this vector It should be made clear that these recommendations are will surely increase with time. not intended to harm aquarium trade activities, because its economic importance for the Minas Gerais State and for Brazil Management recommendations. This study focused on the is undeniable. Instead, they should be seen as a powerful set risk-enhancing role of physical aquarium shops in six cities of tools for disseminating environmental conservation. of Minas Gerais State. The negative consequences of e- Already in the early 1970s, Courtenay et al. (1974) suggested commerce via virtual shops and auctions were not analysed, similar measures for aquarium trade in the state of Florida, but should not be underestimated. For example, Carassius US, in order to prevent non-native ornamental fish species auratus, Cyprinus rubrofuscus, Poecilia latipinna, P. dumping by people practising this hobby. Since our reticulata, Xiphophorus maculatus, X. hellerii, and A. recommendations are more than 35 years late in comparison nigrofasciata are available on e-commerce at very affordable to the US, and the Brazilian culture traditionally remediates prices (Magalhães & Jacobi, 2010). In view of this, the potential environmental disasters rather than prevents them (Guerra, impact of e-commerce as a disseminating source of non-native 1995), it is adviseable that such measures be put in practice species in Minas Gerais State ought to be urgently without delay. Otherwise, the future of many water bodies in investigated. The quantities sold by means of these two types Brazil and especially in Minas Gerais State is foreseeingly of retailing (fixed location and online) should in turn reflect disturbing adding the environmental damages caused by non- the probability of escape from fish farms, a problem which native aquarium fish species to those of ongoing landscape has already caught attention of the Brazilian environmental changes, among which urban pollution, siltation, riparian forest authorities (Magalhães, 2010). destruction, and impoundments. Finally, it should be reminded Brazil is signatory to the Convention on Biological Diversity. that our recommendations were intended for ornamental Article eight of this treaty establishes that each country that is aquarium species, and that other commercially important non- party to the Convention has to make efforts to avoid the native fishes (such as those for human consumption), deserve introduction of non-native species (Alho et al., 2011). One equal attention and specific invasion risk studies. way to greatly reduce the potential impact that aquarium trade 440 Invasion risks posed by ornamental freshwater fish trade

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